8.1: What is an Evolutionary Novelty?

For discrete objects and characters it is easy to see what is new or novel. For example, if I went skydiving, that would be a novel experience for me since I've never been skydiving before. If we put a human on Mars, that would be a novel scientific undertaking for the human race. However, evolution often does not work with discrete characters, instead lines are blurred and fuzzy. For example, we might think of bat wings as a novelty in vertebrates since they are a synapomorphy (shared, derived, defining character) in the bat lineage. Bats invented something new - membranous wings. However, it could also be argued that this is simply a "functional innovation," that is, an elaboration of an existing structure to perform a new function. In this sense, bat wings are simply elongated forelimbs with some extra skin. So what counts as a novelty, exactly? To be direct about it, there really isn't one single definition that can be defended. The confusion seems to stem from our own biases regarding the characters we find interesting and "novel," like feathers, hands, and faces, which all had different evolutionary origins and trajectories.

Given that there isn't a single agreed upon definition of novelty, probably due to the fact that evolution doesn't follow strict patterns, how can we think about this subject at all? In 1963, Ernst Mayr, one of the founders of modern Evolutionary Biology defined a novelty as a new structure or property of an organism that allows it to perform a new function, thus opening a new "adaptive zone". In this reckoning, a novelty allows an organism to exploit a new ecological resource and should lead to an adaptive radiation1. A major flaw in this definition, however, was pointed out in 2008 by Massimo Pigliucci. He noted that some "novelties", like the mammalian inner ear, didn't lead to adaptive radiations and thus wouldn't fall under this definition2. We can broaden the definition to include any character that is unique to a taxon3, however it defies credulity to consider a character like an extra bristle on a crustacean antenna as an evolutionary novelty. Pigliucci combines these two definitions to say that novelties are unique characters that define a taxon that also have a novel function in their ecosystem. This means that they don't necessarily lead to an adaptive radiation, but they still do increase fitness compared to the ancestral state2. I personally like this definition in that it gives us two clear things to look for in a novelty: 1) It's actually new and 2) It does something for the organism. However, this definition is pretty broad and fuzzy. Under it flight feathers in birds, a novelty that allowed them to take to the skies and inhabit the most remote spots on earth, are placed at the same level as a functional protein mutation in a bacterium that gives it 10% greater capacity to digest pesticides.

What is an adaptive radiation?

An adaptive radiation is the rapid evolution of a lineage to fill multiple open ecological niches. One of the most famous adaptive radiations is the evolution of the Galapagos Finches (also called "Darwin's Finches"). When an ancestral population of finches reached the Galapagos Islands the islands had no other similar species with which to compete. The multiple open niches, like feeding on flowering cacti, hard seeds, small seeds, and insects, imposed disruptive selection on the birds. That is, finches with beaks better adapted to eating insects were selected for as were finches with beaks better adapted to eating hard seeds. Finches with intermediate phenotypes (mediocre at eating either food source) were selected against. Over long periods of time, this led to speciation of the finches into at least 12 distinct species each exploiting a slightly different food resource.

One of the luminaries in the field of evolutionary novelty, Gunter Wagner, has created a definition of novelty that can help to direct research programs. His definition is more functional and specific than other definitions. By his reckoning there are two types of novelties:

Type I, a new body part that is not strictly homologous to other body parts and

Type II, a novel variant on a body part that allows for a new function.

A Type II novelty would include the evolution of fins in marine mammals - this is just a reconfiguration of an existing body part. In the case of Type II novelties the homology to ancestral body parts is clear, in a Type I it shouldn't be4. By this definition, we have to decide what we consider to be compelling novelty and what we consider to be compelling evidence. For example, we might decide that mammary glands - derived from hair glands - are novel since we personally feel they have enough differences from hair glands to be independent evolutionary units, but decide that the shiny scales of garfish (ganoid scales) are too similar to standard fish scales to count. In the latter case, we ignore the novel compounds that create the shininess.

Wagner has addressed the problem of using our own perspective to decide what counts as a novelty or not by defining novelties as being associated with novel core Gene-Regulatory-Networks (GRNs). Positional information can vary between species (see the Bicoid example!) but this evolutionarily variable positional information is read out by an evolutionarily stable core-GRN. This core-GRN specifies the tissue by activating "realizer-genes", sometimes called "structural genes". These are the genes that do the business of giving an organ it's functional properties. This realizer-gene output, like the positional information, is also changeable. The realizer-genes can be modified by adaptations to local environments4,5. Since the core-GRN is the stable component of the genetics underlying the development of the novel organ, a novel core-GRN thus is associated with a truly novel organ.

While I truly like this definition because of its simplicity - to understand how novelty arises we just go after those novel core-GRNs that define the novelty - it does have its weaknesses. A technical weakness is that we cannot be sure of the genes that make up a GRN with our current technology. For example, it's easily possible to miss a gene when sequencing transcriptomes, or for plastic developmental programs to compensate for a gene we CRISPR out of the genome. A more philosophical weakness is that in our own hubris it is very easy to shift the boundaries of what we consider to be the core-GRN and equally easy to ignore evidence of the same or similar core-GRNs in clearly non-homologous tissues (like the Notch/Hes interaction being a core-GRN in non-homologous segmentation in some annelids, arthropods, and vertebrates). That said, there does appear to be mounting evidence that, at least in some cases, we can associate a novel organ with a novel core-GRN4.

For now, we will try taking the best of all these definitions to examine some interesting characters that have evolved in various groups. We can even try to define them as novel (or not) by these definitions. We will look at comparative developmental biology and genetics of several key "innovations" (a term that has to do with function rather that distinctiveness). In this chapter, we will look at one ectodermal novelty, insect wings.

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